DOI QR코드

DOI QR Code

Next-generation approaches to the microbial ecology of food fermentations

  • Bokulich, Nicholas A. (Department of Viticulture and Enology, University of California) ;
  • Mills, David A. (Department of Viticulture and Enology, University of California)
  • Received : 2012.05.21
  • Published : 2012.07.31

Abstract

Food fermentations have enhanced human health since the dawn of time and remain a prevalent means of food processing and preservation. Due to their cultural and nutritional importance, many of these foods have been studied in detail using molecular tools, leading to enhancements in quality and safety. Furthermore, recent advances in high-throughput sequencing technology are revolutionizing the study of food microbial ecology, deepening insight into complex fermentation systems. This review provides insight into novel applications of select molecular techniques, particularly next-generation sequencing technology, for analysis of microbial communities in fermented foods. We present a guideline for integrated molecular analysis of food microbial ecology and a starting point for implementing next-generation analysis of food systems.

Keywords

References

  1. Hayes, M., Ross, R. P., Fitzgerald, G. F. and Stanton, C. (2007) Putting microbes to work: dairy fermentation, cell factories and bioactive peptides. Part I: overview. Biotechnol. J. 2, 426-434. https://doi.org/10.1002/biot.200600246
  2. Nout, M. J. (2009) Rich nutrition from the poorest - cereal fermentations in Africa and Asia. Food Microbiol. 26, 685-692. https://doi.org/10.1016/j.fm.2009.07.002
  3. Ross, R. P., Morgan, S. and Hill, C. (2002) Preservation and fermentation: past, present and future. Int. J. Food Microbiol. 79, 3-16. https://doi.org/10.1016/S0168-1605(02)00174-5
  4. Rouse, S. and van Sinderen, D. (2008) Bioprotective potential of lactic acid bacteria in malting and brewing. J. Food Prot. 71, 1724-1733. https://doi.org/10.4315/0362-028X-71.8.1724
  5. Ray, R. C. and Sivakumar, P. S. (2009) Traditional and novel fermented foods and beverages from tropical root and tuber crops: review. Int. J. Food Sci. Technol. 44, 1073-1087. https://doi.org/10.1111/j.1365-2621.2009.01933.x
  6. Tannock, G. W. (2002) Probiotics and prebiotics: Where are we going? (eds.), Caister Academic Press, Norfork, England.
  7. Heard, G. M. and Fleet, G. H. (1986) Evaluation of selective media for enumeration of yeast during wine fermentation. J. Appl. Bacteriol. 60, 477-481. https://doi.org/10.1111/j.1365-2672.1986.tb01086.x
  8. Ampe, F., Omar, N. B., Moizan, C., Wacher, C. and Guyot, J. P. (1999) Polyphasic study of the spatial distribution of microorganisms in mexican pozol, a fermented maize dough, demonstrates the need for cultivation- independent methods to investigate traditional fermentations. Appl. Environ. Microbiol. 65, 5464-5473.
  9. Divol, B. and Lonvaud-Funel, A. (2005) Evidence for viable but nonculturable yeasts in botrytis-affected wine. J. Appl. Microbiol. 99, 85-93. https://doi.org/10.1111/j.1365-2672.2005.02578.x
  10. Millet, V. and Lonvaud-Funel, A. (2000) The viable but non-culturable state of wine micro-organisms during storage. Lett. Appl. Microbiol. 30, 136-141. https://doi.org/10.1046/j.1472-765x.2000.00684.x
  11. Bottari, B., Ercolini, D., Gatti, M. and Neviani, E. (2006) Application of FISH technology for microbiological analysis: current state and prospects. Appl. Microbiol. Biotechnol. 73, 485-494. https://doi.org/10.1007/s00253-006-0615-z
  12. Andorra, I., Monteiro, M., Esteve-Zarzoso, B., Albergaria, H. and Mas, A. (2011) Analysis and direct quantification of Saccharomyces cerevisiae and Hanseniaspora guilliermondii populations during alcoholic fermentation by fluorescence in situ hybridization, flow cytometry and quantitative PCR. Food Microbiol. 28, 1483-1491. https://doi.org/10.1016/j.fm.2011.08.009
  13. Xufre, A., Albergaria, H., Inacio, J., Spencer-Martins, I. and Girio, F. (2006) Application of fluorescence in situ hybridisation (FISH) to the analysis of yeast population dynamics in winery and laboratory grape must fermentations. Int. J. Food Microbiol. 108, 376-384.
  14. Blasco, L., Ferrer, S. and Pardo, I. (2003) Development of specific fluorescent oligonucleotide probes for in situ identification of wine lactic acid bacteria. FEMS Microbiol. Lett. 225, 115-123. https://doi.org/10.1016/S0378-1097(03)00501-9
  15. Yasuhara, T., Yuuki, T. and Kagami, N. (2001) Novel quantitative method for detection of Pectinatus using rRNA targeted fluorescent probes. J. Am. Soc. Brew. Chem. 59, 117-121.
  16. Babot, J. D., Hidalgo, M., Arganaraz-Martinez, E., Apella, M. C. and Perez Chaia, A. (2011) Fluorescence in situ hybridization for detection of classical propionibacteria with specific 16S rRNA-targeted probes and its application to enumeration in Gruyere cheese. Int. J. Food Microbiol. 145, 221-228. https://doi.org/10.1016/j.ijfoodmicro.2010.12.024
  17. Bottari, B., Santarelli, M., Neviani, E. and Gatti, M. (2010) Natural whey starter for Parmigiano Reggiano: culture-independent approach. J. Appl. Microbiol. 108, 1676-1684. https://doi.org/10.1111/j.1365-2672.2009.04564.x
  18. Mounier, J., Monnet, C., Jacques, N., Antoinette, A. and Irlinger, F. (2009) Assessment of the microbial diversity at the surface of Livarot cheese using culture-dependent and independent approaches. Int. J. Food Microbiol. 133, 31-37. https://doi.org/10.1016/j.ijfoodmicro.2009.04.020
  19. Ercolini, D., Hill, P. J. and Dodd, C. E. (2003) Development of a fluorescence in situ hybridization method for cheese using a 16S rRNA probe. J. Microbiol. Methods 52, 267-271. https://doi.org/10.1016/S0167-7012(02)00162-8
  20. Klug, B., Rodler, C., Koller, M., Wimmer, G., Kessler, H. H., Grube, M. and Santigli, E. (2011) Oral biofilm analysis of palatal expanders by fluorescence in-situ hybridization and confocal laser scanning microscopy. J. Vis. Exp. 20, 2967.
  21. Postollec, F., Falentin, H., Pavan, S., Combrisson, J. and Sohier, D. (2011) Recent advances in quantitative PCR (qPCR) applications in food microbiology. Food Microbiol. 28, 848-861. https://doi.org/10.1016/j.fm.2011.02.008
  22. Lucas, P. M., Claisse, O. and Lonvaud-Funel, A. (2008) High frequency of histamine-producing bacteria in the enological environment and instability of the histidine decarboxylase production phenotype. Appl. Environ. Microbiol. 74, 811-817. https://doi.org/10.1128/AEM.01496-07
  23. Arena, M. P., Romano, A., Capozzi, V., Beneduce, L., Ghariani, M., Grieco, F., Lucas, P. and Spano, G. (2011) Expression of Lactobacillus brevis IOEB 9809 tyrosine decarboxylase and agmatine deiminase genes in wine correlates with substrate availability. Lett. Appl. Microbiol. 53, 395-402. https://doi.org/10.1111/j.1472-765X.2011.03120.x
  24. Ladero, V., Coton, M., Fernandez, M., Buron, N., Cruz Martin, M., Guichard, H., Coton, E. and Alvarez, M. A. (2011) Biogenic amines content in Spanish and French natural ciders: Application of qPCR for quantitative detection of biogenic amine-producers. Food Microbiol. 28, 554-561. https://doi.org/10.1016/j.fm.2010.11.005
  25. Fernandez, M., del Rio, B., Linares, D. M., Martin, M. C. and Alvarez, M. A. (2006) Real-time polymerase chain reaction for quantitative detection of histamine-producing bacteria: use in cheese production. J. Dairy Sci. 89, 3763-3769. https://doi.org/10.3168/jds.S0022-0302(06)72417-1
  26. Torriani, S., Gatto, V., Sembeni, S., Tofalo, R., Suzzi, G., Belletti, N., Gardini, F. and Bover-Cid, S. (2008) Rapid detection and quantification of tyrosine decarboxylase gene (tdc) and its expression in gram-positive bacteria associated with fermented foods using PCR-based methods. J. Food Prot. 71, 93-101. https://doi.org/10.4315/0362-028X-71.1.93
  27. Ibarburu, I., Aznar, R., Elizaquivel, P., Garcia-Quintans, N., Lopez, P., Munduate, A., Irastorza, A. and Duenas, M. T. (2010) A real-time PCR assay for detection and quantification of 2-branched (1,3)-$\beta$-D-glucan producing lactic acid bacteria in cider. Int. J. Food Microbiol. 143, 26-31. https://doi.org/10.1016/j.ijfoodmicro.2010.07.023
  28. Mendes-Ferreira, A., Barbosa, C., Jimenez-Marti, E., Del Olmo, M. L. and Mendes-Faia, A. (2010) The wine yeast strain-dependent expression of genes implicated in sulfide production in response to nitrogen availability. J. Microbiol. Biotechnol. 20, 1314-1321. https://doi.org/10.4014/jmb.1003.03039
  29. Haakensen, M. C., Butt, L., Chaban, B., Deneer, H., Ziola, B. and Dowgiert, T. (2007) horA-Speciric real-time PCR for detection of beer-spoilage lactic acid bacteria. J. Am. Soc. Brew. Chem. 65, 157-165.
  30. Cho, G. S., Krauss, S., Huch, M., Du Toit, M. and Franz, C. M. (2011) Development of a quantitative PCR for detection of Lactobacillus plantarum starters during wine malolactic fermentation. J. Microbiol. Biotechnol. 21, 1280-1286. https://doi.org/10.4014/jmb.1107.07003
  31. Muyzer, G., Dewaal, E. C. and Uitterlinden, A. G. (1993) Profiling of complex microbial populations by denaturing gradient gel-electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S ribosomal RNA. Appl. Environ. Microbiol. 59, 695-700.
  32. Kisand, V. and Wikner, J. (2003) Limited resolution of 16S rDNA DGGE caused by melting properties and closely related DNA sequences. J. Microbiol. Meth. 54, 183-191. https://doi.org/10.1016/S0167-7012(03)00038-1
  33. Sekiguchi, H., Tomioka, N., Nakahara, T. and Uchiyama, H. (2001) A single band does not always represent single bacterial strains in denaturing gradient gel electrophoresis analysis. Biotechnol. Lett. 23, 1205-1208. https://doi.org/10.1023/A:1010517117046
  34. Nubel, U., Engelen, B., Felske, A., Snaidr, J., Wieshuber, A., Amann, R. I., Ludwig, W. and Backhaus, H. (1996) Sequence heterogeneities of genes encoding 16S rRNAs in Paenibacillus polymyxa detected by temperature gradient gel electrophoresis. J. Bacteriol. 178, 5636-5643. https://doi.org/10.1128/jb.178.19.5636-5643.1996
  35. Polz, M. F. and Cavanaugh, C. M. (1998) Bias in template- to-product ratios in multitemplate PCR. Appl. Environ. Microbiol. 64, 3724-3730.
  36. Speksnijder, A., Kowalchuk, G. A., De Jong, S., Kline, E., Stephen, J. R. and Laanbroek, H. J. (2001) Microvariation artifacts introduced by PCR and cloning of closely related 16S rRNA gene sequences. Appl. Environ. Microbiol. 67, 469-472. https://doi.org/10.1128/AEM.67.1.469-472.2001
  37. Tourlomousis, P., Kemsley, E. K., Ridgway, K. P., Toscano, M. J., Humphrey, T. J. and Narbad, A. (2010) PCR-denaturing gradient gel electrophoresis of complex microbial communities: a two-step approach to address the effect of gel-to-gel variation and allow valid comparisons across a large dataset. Microb. Ecol. 59, 776-786. https://doi.org/10.1007/s00248-009-9613-x
  38. Cocolin, L., Bisson, L. F. and Mills, D. A. (2000) Direct profiling of the yeast dynamics in wine fermentations. FEMS Microbiol. Lett. 189, 81-87. https://doi.org/10.1111/j.1574-6968.2000.tb09210.x
  39. Renouf, V., Claisse, O., Miot-Sertier, C. and Lonvaud- Funel, A. (2006) Lactic acid bacteria evolution during winemaking: use of rpoB gene as a target for PCR-DGGE analysis. Food Microbiol. 23, 136-145. https://doi.org/10.1016/j.fm.2005.01.019
  40. Ercolini, D. (2004) PCR-DGGE fingerprinting: novel strategies for detection of microbes in food. J. Microbiol. Meth. 56, 297-314. https://doi.org/10.1016/j.mimet.2003.11.006
  41. Kaplan, C. W. and Kitts, C. L. (2003) Variation between observed and true Terminal Restriction Fragment length is dependent on true TRF length and purine content. J. Microbiol. Meth. 54, 121-125. https://doi.org/10.1016/S0167-7012(03)00003-4
  42. Marsh, T. L. (2005) Culture-independent microbial community analysis with terminal restriction fragment length polymorphism. Methods Enzymol. 397, 308-329. https://doi.org/10.1016/S0076-6879(05)97018-3
  43. Hartmann, M., Enkerli, J. and Widmer, F. (2007) Residual polymerase activity-induced bias in terminal restriction fragment length polymorphism analysis. Env. Microbiol. 9, 555-559. https://doi.org/10.1111/j.1462-2920.2006.01169.x
  44. Egert, M. and Friedrich, M. W. (2003) Formation of pseudo- terminal restriction fragments, a PCR-related bias affecting terminal restriction fragment length polymorphism analysis of microbial community structure. Appl. Environ. Microbiol. 69, 2555-2562. https://doi.org/10.1128/AEM.69.5.2555-2562.2003
  45. Bokulich, N. A. and Mills, D. A. (2012) Differentiation of mixed lactic acid bacteria communities in beverage fermentations using targeted terminal restriction fragment length polymorphism. Food Microbiol. 31, 126-132. doi:10.1016/j.fm.2012.02.007.
  46. Culman, S. W., Gauch, H. G., Blackwood, C. B. and Thies, J. E. (2008) Analysis of T-RFLP data using analysis of variance and ordination methods: A comparative study. J. Microbiol. Meth. 75, 55-63. https://doi.org/10.1016/j.mimet.2008.04.011
  47. Blackwood, C. B., Marsh, T. L., Kim, S. H. and Paul, E. A. (2003) Terminal restriction fragment length polymorphism data analysis for quantitative comparison of microbial communities. Appl. Environ. Microbiol. 69, 926-932. https://doi.org/10.1128/AEM.69.2.926-932.2003
  48. Blackwood, C. B., Hudleston, D., Zak, D. R. and Buyer, J. S. (2007) Interpreting ecological diversity indices applied to terminal restriction fragment length polymorphism data: insights from simulated microbial communities. Appl. Environ. Microbiol. 73, 5276-5283. https://doi.org/10.1128/AEM.00514-07
  49. Schutte, U. M. E., Abdo, Z., Bent, S. J., Shyu, C., Williams, C. J., Pierson, J. D. and Forney, L. J. (2008) Advances in the use of terminal restriction fragment length polymorphism (T-RFLP) analysis of 16S rRNA genes to characterize microbial communities. Appl. Microbiol. Biotechnol. 80, 365-380. https://doi.org/10.1007/s00253-008-1565-4
  50. Liu, W. T., Marsh, T. L., Cheng, H. and Forney, L. J. (1997) Characterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16S rRNA. Appl. Environ. Microbiol. 63, 4516-4522.
  51. Rademaker, J. L. W., Hoolwerf, J. D., Wagendorp, A. A. and te Giffel, M. C. (2006) Assessment of microbial population dynamics during yoghurt and hard cheese fermentation and ripening by DNA population fingerprinting. Int. Dairy J. 16, 457-466. https://doi.org/10.1016/j.idairyj.2005.05.009
  52. Rademaker, J. L. W., Peinhopf, M., Rijnen, L., Bockelmann, W. and Noordman, W. H. (2005) The surface microflora dynamics of bacterial smear-ripened Tilsit cheese determined by T-RFLP DNA population fingerprint analysis. Int. Dairy J. 15, 785-794. https://doi.org/10.1016/j.idairyj.2004.08.027
  53. Sanchez, J. I., Rossetti, L., Martinez, B., Rodriguez, A. and Giraffa, G. (2006) Application of reverse transcriptase PCR-based T-RFLP to perform semi-quantitative analysis of metabolically active bacteria in dairy fermentations. J. Microbiol. Meth. 65, 268-277. https://doi.org/10.1016/j.mimet.2005.07.018
  54. Bokulich, N. A., Hwang, C. F., Liu, S., Boundy-Mills, K. and Mills, D. A. (2012) Profiling the yeast communities of wine using terminal restriction fragment length polymorphism. Am. J. Enol. Vitic. 63, doi:10.5344/ajev.2011.11077.
  55. Bokulich, N. A., Bamforth, C. W. and Mills, D. A. (2012) Brewhouse-resident microbiota are responsible for multi- stage fermentation of american coolship ale. PLoS ONE 7, e35507. doi:10.1371/journal.pone.0035507.
  56. Bokulich, N. A., Joseph, C. M. L., Allen, G., Benson, A. K. and Mills, D. A. (2012) Next-Generation Sequencing Reveals Significant Bacterial Diversity of Botrytized Wine. PLoS ONE 7, e36357. doi:10.1371/journal.pone.0036357.
  57. Marcobal, A., Underwood, M. and Mills, D. A. (2008) Rapid determination of the bacterial composition of commercial probiotic products by terminal restriction fragment length polymorphism analysis. J. Pediatr. Gastroenterol. Nutr. 46, 608-611. https://doi.org/10.1097/MPG.0b013e3181660694
  58. Margulies, M., Egholm, M., Altman, W. E., Attiya, S., Bader, J. S., Bemben, L. A., Berka, J., Braverman, M. S., Chen, Y. J., Chen, Z., Dewell, S. B., Du, L., Fierro, J. M., Gomes, X. V., Godwin, B. C., He, W., Helgesen, S., Ho, C. H., Irzyk, G. P., Jando, S. C., Alenquer, M. L., Jarvie, T. P., Jirage, K. B., Kim, J. B., Knight, J. R., Lanza, J. R., Leamon, J. H., Lefkowitz, S. M., Lei, M., Li, J., Lohman, K. L., Lu, H., Makhijani, V. B., McDade, K. E., McKenna, M. P., Myers, E. W., Nickerson, E., Nobile, J. R., Plant, R., Puc, B. P., Ronan, M. T., Roth, G. T., Sarkis, G. J., Simons, J. F., Simpson, J. W., Srinivasan, M., Tartaro, K. R., Tomasz, A., Vogt, K. A., Volkmer, G. A., Wang, S. H., Wang, Y., Weiner, M. P., Yu, P., Begley, R. F. and Rothberg, J. M. (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437, 376-380.
  59. Bennett, S. (2004) Solexa Ltd. Pharmacogenomics 5, 433-438. https://doi.org/10.1517/14622416.5.4.433
  60. Kuczynski, J., Lauber, C. L., Walters, W. A., Parfrey, L. W., Clemente, J. C., Gevers, D. and Knight, R. (2012) Experimental and analytical tools for studying the human microbiome. Nat. Rev. Genet. 13, 47-58. https://doi.org/10.1038/nrg3129
  61. Liu, Z., Lozupone, C. A., Hamady, M., Bushman, F. D. and Knight, R. (2007) Short pyrosequencing reads suffice for accurate microbial community analysis. Nucleic Acids. Res. 35, e120. https://doi.org/10.1093/nar/gkm541
  62. Kiyohara, M., Koyanagi, T., Matsui, H., Yamamoto, K., Take, H., Katsuyama, Y., Tsuji, A., Miyamae, H., Kondo, T., Nakamura, S., Katayama, T. and Kumagai, H. (2012) Changes in microbiota population during fermentation of narezushi as revealed by pyrosequencing analysis. Biosci. Biotechnol. Biochem. 76, 48-52. https://doi.org/10.1271/bbb.110424
  63. Koyanagi, T., Kiyohara, M., Matsui, H., Yamamoto, K., Kondo, T., Katayama, T. and Kumagai, H. (2011) Pyrosequencing survey of the microbial diversity of 'narezushi', an archetype of modern Japanese sushi. Lett. Appl. Microbiol. 53, 635-640. https://doi.org/10.1111/j.1472-765X.2011.03155.x
  64. Sakamoto, N., Tanaka, S., Sonomoto, K. and Nakayama, J. (2011) 16S rRNA pyrosequencing-based investigation of the bacterial community in nukadoko, a pickling bed of fermented rice bran. Int. J. Food Microbiol. 144, 352-359. https://doi.org/10.1016/j.ijfoodmicro.2010.10.017
  65. Li, X. R., Ma, E. B., Yan, L. Z., Meng, H., Du, X. W., Zhang, S. W. and Quan, Z. X. (2011) Bacterial and fungal diversity in the traditional Chinese liquor fermentation process. Int. J. Food Microbiol. 146, 31-37. https://doi.org/10.1016/j.ijfoodmicro.2011.01.030
  66. Alegria, A., Szczesny, P., Mayo, B., Bardowski, J. and Kowalczyk, M. (2012) Biodiversity in Oscypek, a traditional Polish cheese, determined by culture-dependent and -independent approaches. Appl. Environ. Microbiol. 78, 1890-1898. https://doi.org/10.1128/AEM.06081-11
  67. Humblot, C. and Guyot, J. P. (2009) Pyrosequencing of tagged 16S rRNA gene amplicons for rapid deciphering of the microbiomes of fermented foods such as pearl millet slurries. Appl. Environ. Microbiol. 75, 4354-4361. https://doi.org/10.1128/AEM.00451-09
  68. Roh, S. W., Kim, K. H., Nam, Y. D., Chang, H. W., Park, E. J. and Bae, J. W. (2010) Investigation of archaeal and bacterial diversity in fermented seafood using barcoded pyrosequencing. ISME J. 4, 1-16. https://doi.org/10.1038/ismej.2009.83
  69. Jung, M. J., Nam, Y. D., Roh, S. W. and Bae, J. W. (2012) Unexpected convergence of fungal and bacterial communities during fermentation of traditional Korean alcoholic beverages inoculated with various natural starters. Food Microbiol. 30, 112-123. https://doi.org/10.1016/j.fm.2011.09.008
  70. Kim, Y. S., Kim, M. C., Kwon, S. W., Kim, S. J., Park, I. C., Ka, J. O. and Weon, H. Y. (2011) Analyses of bacterial communities in meju, a Korean traditional fermented soybean bricks, by cultivation-based and pyrosequencing methods. J. Microbiol. 49, 340-348. https://doi.org/10.1007/s12275-011-0302-3
  71. Nam, Y. D., Lee, S. Y. and Lim, S. I. (2012) Microbial community analysis of Korean soybean pastes by next-generation sequencing. Int. J. Food Microbiol. 155, 36-42. https://doi.org/10.1016/j.ijfoodmicro.2012.01.013
  72. Nam, Y. D., Park, S. L. and Lim, S. I. (2012) Microbial Composition of the Korean Traditional Food "kochujang" Analyzed by a Massive Sequencing Technique. J. Food Sci. 77, M250-256. https://doi.org/10.1111/j.1750-3841.2012.02656.x
  73. Park, E. J., Chun, J., Cha, C. J., Park, W. S., Jeon, C. O. and Bae, J. W. (2012) Bacterial community analysis during fermentation of ten representative kinds of kimchi with barcoded pyrosequencing. Food Microbiol. 30, 197-204. https://doi.org/10.1016/j.fm.2011.10.011
  74. Park, E. J., Kim, K. H., Abell, G. C., Kim, M. S., Roh, S. W. and Bae, J. W. (2011) Metagenomic analysis of the viral communities in fermented foods. Appl. Environ Microbiol. 77, 1284-1291. https://doi.org/10.1128/AEM.01859-10
  75. Lozupone, C. A. and Knight, R. (2005) UniFrac: A new phylogenetic method for comparing microbial communities. Appl. Environ. Microbiol. 71, 8228-8235. https://doi.org/10.1128/AEM.71.12.8228-8235.2005
  76. Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., Fierer, N., Gonzalez Pena, A., Goodrich, J. K., Gordon, J. I., Huttley, G. A., Kelley, S. T., Knights, D., Koenig, J. E., Ley, R. E., Lozupone, C. A., McDonald, D., Muegge, B. D., Pirrung, M., Reeder, J., Sevinsky, J. R., Turnbaugh, P. J., Walters, W. A., Widmann, J., Yatsunenko, T., Zaneveld, J. and Knight, R. (2010) Qiime allows analysis of high-throughput community sequence data. Nat. Methods 7, 335-336. https://doi.org/10.1038/nmeth.f.303
  77. Schloss, P. D., Westcott, S. L., Ryabin, T., Hall, J. R., Hartmann, M., Hollister, E. B., Lesniewski, R. A., Oakley, B. B., Parks, D. H., Robinson, C. J., Sahl, J. W., Stres, B., Thallinger, G. G., Van Horn, D. J. and Weber, C. F. (2009) Introducing mothur: open-source, platform- independent, community-supported software for describing and comparing microbial communities. Appl. Environ Microbiol. 75, 7537-7541. https://doi.org/10.1128/AEM.01541-09
  78. Zaneveld, J. R., Parfrey, L. W., Van Treuren, W., Lozupone, C., Clemente, J. C., Knights, D., Stombaugh, J., Kuczynski, J. and Knight, R. (2011) Combined phylogenetic and genomic approaches for the high-throughput study of microbial habitat adaptation. Trends Microbiol. 19, 472-482. https://doi.org/10.1016/j.tim.2011.07.006
  79. Nilsson, R. H., Ryberg, M., Kristiansson, E., Abarenkov, K., Larsson, K. H. and Koljalg, U. (2006) Taxonomic reliability of DNA sequences in public sequence databases: a fungal perspective. PLoS ONE 1, e59. https://doi.org/10.1371/journal.pone.0000059
  80. Tedersoo, L., Abarenkov, K., Nilsson, R. H., Schussler, A., Grelet, G. A., Kohout, P., Oja, J., Bonito, G. M., Veldre, V., Jairus, T., Ryberg, M., Larsson, K. H. and Koljalg, U. (2011) Tidying up international nucleotide sequence databases: ecological, geographical and sequence quality annotation of its sequences of mycorrhizal fungi. PLoS ONE 6, e24940. https://doi.org/10.1371/journal.pone.0024940
  81. McDonald, D., Price, M. N., Goodrich, J., Nawrocki, E. P., DeSantis, T. Z., Probst, A., Andersen, G. L., Knight, R. and Hugenholtz, P. (2012) An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J. 6, 610-618. https://doi.org/10.1038/ismej.2011.139
  82. De Santis, T., Hugenholtz, P., Larsen, N., Rojas, N., Brodie, E., Keller, K., Huber, T., Dalevi, D., Hu, P. and Andersen, G. L. (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 72, 5069-5072. https://doi.org/10.1128/AEM.03006-05
  83. Pruesse, E., Quast, C., Knittel, K., Fuchs, B. M., Ludwig, W., Peplies, J. and Glockner, F. O. (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids. Res. 35, 7188-7196. https://doi.org/10.1093/nar/gkm864
  84. Cole, J. R., Wang, Q., Cardenas, E., Fish, J., Chai, B., Farris, R. J., Kulam-Syed-Mohideen, A. S., McGarrel, D. M., Marsh, T. L., Garrity, G. M. and Tiedje, J. M. (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids. Res. 37, D141-D145. https://doi.org/10.1093/nar/gkn879
  85. Abarenkov, K., Nilsson, R. H., Larsson, K.-H., Alexander, I. J., Eberhardt, U., Erland, S., Høiland, K., Kjøller, R., Larsson, E., Pennanen, T., Sen, R., Taylor, A. F. S., Tedersoo, L., Ursing, B. M., Vrålstad, T., Liimatainen, K., Peintner, U. and Kõljalg, U. (2010) The UNITE database for molecular identification of fungi - recent updates and future perspectives. New Phytol. 186, 1447-1452.
  86. Soergel, D. A. W., Dey, N., Knight, R. and Brenner, S. E. (2012) Selection of primers for optimal taxonomic classification of environmental 16S rRNA gene sequences. ISME J. 7, doi: 10.1038/ismej.2011.208.
  87. Nilsson, R. H., Kristiansson, E., Ryberg, M., Hallenberg, N. and Larsson, K. H. (2008) Intraspecific ITS variability in the kingdom fungi as expressed in the international sequence databases and its implications for molecular species identification. Evol. Bioinform. Online 4, 193-201.
  88. Simon, C. and Daniel, R. (2011) Metagenomic analyses: past and future trends. Appl. Environ. Microbiol. 77, 1153-1161. https://doi.org/10.1128/AEM.02345-10
  89. Lauber, C. L., Zhou, N., Gordon, J. I., Knight, R. and Fierer, N. (2010) Effect of storage conditions on the assessment of bacterial community structure in soil and human-associated samples. FEMS Microbiol. Lett. 307, 80-86. https://doi.org/10.1111/j.1574-6968.2010.01965.x
  90. Li, F., Hullar, M. A. and Lampe, J. W. (2007) Optimization of terminal restriction fragment polymorphism (TRFLP) analysis of human gut microbiota. J. Microbiol. Meth. 68, 303-311. https://doi.org/10.1016/j.mimet.2006.09.006
  91. Rossen, L., Norskov, P., Holmstrom, K. and Rasmussen, O. F. (1992) Inhibition of PCR by components of food samples, microbial diagnostic assays and DNA-extraction solutions. Int. J. Food Microbiol. 17, 37-45. https://doi.org/10.1016/0168-1605(92)90017-W
  92. Nocker, A., Cheung, C. Y. and Camper, A. K. (2006) Comparison of propidium monoazide with ethidium monoazide for differentiation of live vs. dead bacteria by selective removal of DNA from dead cells. J. Microbiol. Meth. 67, 310-320. https://doi.org/10.1016/j.mimet.2006.04.015
  93. Nocker, A., Richter-Heitmann, T., Montijn, R., Schuren, F. and Kort, R. (2010) Discrimination between live and dead cells in bacterial communities from environmental water samples analyzed by 454 pyrosequencing. Int. Microbiol. 13, 59-65.
  94. Andorra, I., Esteve-Zarzoso, B., Guillamon, J. M. and Mas, A. (2010) Determination of viable wine yeast using DNA binding dyes and quantitative PCR. Int. J. Food Microbiol. 144, 257-262. https://doi.org/10.1016/j.ijfoodmicro.2010.10.003
  95. Anderson, I. C. and Cairney, J. W. G. (2004) Diversity and ecology of soil fungal communities: increased understanding through the application of molecular techniques. Env. Microbiol. 6, 769-779. https://doi.org/10.1111/j.1462-2920.2004.00675.x
  96. Kurtzman, C. and Robnett, C. J. (1998) Identification and phylogeny of ascomycetous yeasts from analysis of nuclear large subunit (26S) ribosomal DNA partial sequences. Antonie van Leeuwenhoek 73, 331-371. https://doi.org/10.1023/A:1001761008817
  97. Schoch, C. L., Seifert, K. A., Huhndorf, S., Robert, V., Spouge, J. L., Levesque, C. A. and Chen, W. (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. PNAS 109, 6241-6246. https://doi.org/10.1073/pnas.1117018109
  98. Nilsson, R. H., Ryberg, M., Abarenkov, K., Sjokvist, E. and Kristiansson, E. (2009) The ITS region as a target for characterization of fungal communities using emerging sequencing technologies. FEMS Microbiol. Lett. 296, 97-101. https://doi.org/10.1111/j.1574-6968.2009.01618.x
  99. Bellemain, E., Carlsen, T., Brochmann, C., Coissac, E., Taberlet, P. and Kauserud, H. (2010) ITS as an environmental DNA barcode for fungi: an in silico approach reveals potential PCR biases. BMC Microbiol. 10, 189. https://doi.org/10.1186/1471-2180-10-189
  100. Sakai, M., Matsuka, A., Komura, T. and Kanazawa, S. (2004) Application of a new PCR primer for terminal restriction fragment length polymorphism analysis of the bacterial communities in plant roots. J. Microbiol. Methods. 59, 81-89. https://doi.org/10.1016/j.mimet.2004.06.005
  101. Martin, K. J. and Rygiewicz, P. T. (2005) Fungal-specific PCR primers developed for analysis of the ITS region of environmental DNA extracts. BMC Microbiol. 5, 28. https://doi.org/10.1186/1471-2180-5-28
  102. Sakamoto, N., Tanaka, S., Sonomoto, K. and Nakayama, J. (2011) 16S rRNA pyrosequencing-based investigation of the bacterial community in nukadoko, a pickling bed of fermented rice bran. Int. J. Food Microbiol. 144, 352-359. https://doi.org/10.1016/j.ijfoodmicro.2010.10.017
  103. Kruger, D., Kapturska, D., Fischer, C., Daniel, R. and Wubet, T. (2012) Diversity Measures in Environmental Sequences Are Highly Dependent on Alignment Quality-Data from ITS and New LSU Primers Targeting Basidiomycetes. PLoS ONE 7, e32139. https://doi.org/10.1371/journal.pone.0032139

Cited by

  1. Diversity of the microbiota involved in wine and organic apple cider submerged vinegar production as revealed by DHPLC analysis and next-generation sequencing vol.223, 2016, https://doi.org/10.1016/j.ijfoodmicro.2016.02.007
  2. FT-IR spectroscopy: A powerful tool for studying the inter- and intraspecific biodiversity of cultivable non-Saccharomyces yeasts isolated from grape must vol.121, 2016, https://doi.org/10.1016/j.mimet.2015.12.009
  3. Comparative microbiota assessment of wilted Italian ryegrass, whole crop corn, and wilted alfalfa silage using denaturing gradient gel electrophoresis and next-generation sequencing vol.101, pp.4, 2017, https://doi.org/10.1007/s00253-016-7900-2
  4. Microbial diversity and metabolite composition of Belgian red-brown acidic ales vol.221, 2016, https://doi.org/10.1016/j.ijfoodmicro.2015.12.009
  5. Cheese rind microbial communities: diversity, composition and origin vol.362, pp.2, 2015, https://doi.org/10.1093/femsle/fnu015
  6. Strategies to develop strain-specific PCR based assays for probiotics vol.6, pp.6, 2015, https://doi.org/10.3920/BM2015.0009
  7. Unraveling Core Functional Microbiota in Traditional Solid-State Fermentation by High-Throughput Amplicons and Metatranscriptomics Sequencing vol.8, 2017, https://doi.org/10.3389/fmicb.2017.01294
  8. Mapping microbial ecosystems and spoilage-gene flow in breweries highlights patterns of contamination and resistance vol.4, 2015, https://doi.org/10.7554/eLife.04634
  9. Cheese surface microbiota complexity: RT-PCR-DGGE, a tool for a detailed picture? vol.162, pp.1, 2013, https://doi.org/10.1016/j.ijfoodmicro.2012.12.009
  10. Three-phase succession of autochthonous lactic acid bacteria to reach a stable ecosystem within 7 days of natural bamboo shoot fermentation as revealed by different molecular approaches vol.24, pp.13, 2015, https://doi.org/10.1111/mec.13237
  11. Molecular Methods in Food Safety Microbiology: Interpretation and Implications of Nucleic Acid Detection vol.13, pp.4, 2014, https://doi.org/10.1111/1541-4337.12072
  12. Exploring the Sources of Bacterial Spoilers in Beefsteaks by Culture-Independent High-Throughput Sequencing vol.8, pp.7, 2013, https://doi.org/10.1371/journal.pone.0070222
  13. Use of a metagenetic approach to monitor the bacterial microbiota of “Tomme d'Orchies” cheese during the ripening process vol.247, 2017, https://doi.org/10.1016/j.ijfoodmicro.2016.10.034
  14. Fermented Foods as Experimentally Tractable Microbial Ecosystems vol.161, pp.1, 2015, https://doi.org/10.1016/j.cell.2015.02.034
  15. Effects of Inoculated Starter of Lactic Acid Bacteria on Quality and Microbial Diversity of Pickled Wax Gourd in Eastern Zhejiang vol.41, pp.2, 2017, https://doi.org/10.1111/jfpp.12833
  16. PNAS Plus: From the Cover: Microbial biogeography of wine grapes is conditioned by cultivar, vintage, and climate vol.111, pp.1, 2014, https://doi.org/10.1073/pnas.1317377110
  17. Microbial bioinformatics for food safety and production vol.17, pp.2, 2016, https://doi.org/10.1093/bib/bbv034
  18. Fungal diversity of “Tomme d'Orchies” cheese during the ripening process as revealed by a metagenomic study vol.258, 2017, https://doi.org/10.1016/j.ijfoodmicro.2017.07.015
  19. Analysis of Bacterial Community Composition of Corroded Steel Immersed in Sanya and Xiamen Seawaters in China via Method of Illumina MiSeq Sequencing vol.8, 2017, https://doi.org/10.3389/fmicb.2017.01737
  20. Probiotics and gut health in infants: A preliminary case–control observational study about early treatment with Lactobacillus reuteri DSM 17938 vol.451, 2015, https://doi.org/10.1016/j.cca.2015.02.027
  21. Monitoring Seasonal Changes in Winery-Resident Microbiota vol.8, pp.6, 2013, https://doi.org/10.1371/journal.pone.0066437
  22. Microbiota characterization of a Belgian protected designation of origin cheese, Herve cheese, using metagenomic analysis vol.97, pp.10, 2014, https://doi.org/10.3168/jds.2014-8225
  23. Insights into the microbial diversity and community dynamics of Chinese traditional fermented foods from using high-throughput sequencing approaches vol.18, pp.4, 2017, https://doi.org/10.1631/jzus.B1600148
  24. A new perspective on microbial landscapes within food production vol.37, 2016, https://doi.org/10.1016/j.copbio.2015.12.008
  25. Analysis of microbial community variation during the mixed culture fermentation of agricultural peel wastes to produce lactic acid vol.208, 2016, https://doi.org/10.1016/j.biortech.2016.02.054
  26. Bacterial diversity of the Colombian fermented milk “Suero Costeño” assessed by culturing and high-throughput sequencing and DGGE analysis of 16S rRNA gene amplicons vol.68, 2017, https://doi.org/10.1016/j.fm.2017.07.011
  27. Foodomics: A novel approach for food microbiology 2017, https://doi.org/10.1016/j.trac.2017.05.012
  28. The fungal community structure of barley malts from diverse geographical regions correlates with malt quality parameters vol.215, 2015, https://doi.org/10.1016/j.ijfoodmicro.2015.08.019
  29. Tracing microbiota changes inyamahai-moto, the traditional Japanese sake starter vol.80, pp.2, 2016, https://doi.org/10.1080/09168451.2015.1095067
  30. Recent transcriptomics advances and emerging applications in food science vol.52, 2013, https://doi.org/10.1016/j.trac.2013.06.014
  31. Characterization of the bacterial biodiversity in Pico cheese (an artisanal Azorean food) vol.192, 2015, https://doi.org/10.1016/j.ijfoodmicro.2014.09.031
  32. Improved Selection of Internal Transcribed Spacer-Specific Primers Enables Quantitative, Ultra-High-Throughput Profiling of Fungal Communities vol.79, pp.8, 2013, https://doi.org/10.1128/AEM.03870-12
  33. High-Throughput Sequencing and Metagenomics: Moving Forward in the Culture-Independent Analysis of Food Microbial Ecology vol.79, pp.10, 2013, https://doi.org/10.1128/AEM.00256-13
  34. Facility-Specific “House” Microbiome Drives Microbial Landscapes of Artisan Cheesemaking Plants vol.79, pp.17, 2013, https://doi.org/10.1128/AEM.00934-13
  35. The Microbiology of Malting and Brewing vol.77, pp.2, 2013, https://doi.org/10.1128/MMBR.00060-12
  36. Indigenous Bacteria and Fungi Drive Traditional Kimoto Sake Fermentations vol.80, pp.17, 2014, https://doi.org/10.1128/AEM.00663-14
  37. Temporal and Spatial Differences in Microbial Composition during the Manufacture of a Continental-Type Cheese vol.81, pp.7, 2015, https://doi.org/10.1128/AEM.04054-14
  38. 伝統発酵食品中に築かれる細菌叢の変遷と多様性 vol.28, pp.2, 2017, https://doi.org/10.4109/jslab.28.84
  39. Bacterial Communities in Serpa Cheese by Culture Dependent Techniques, 16S rRNA Gene Sequencing and High-throughput Sequencing Analysis vol.83, pp.5, 2018, https://doi.org/10.1111/1750-3841.14141
  40. Microbial community dynamics of a blue-veined raw milk cheese from the United Kingdom vol.101, pp.6, 2018, https://doi.org/10.3168/jds.2017-14104
  41. Microbiome dynamics during ensiling of corn with and without Lactobacillus plantarum inoculant vol.102, pp.9, 2018, https://doi.org/10.1007/s00253-018-8903-y
  42. 16S rRNA Gene Primer Validation for Bacterial Diversity Analysis of Vegetable Products vol.81, pp.5, 2018, https://doi.org/10.4315/0362-028X.JFP-17-346
  43. Modulation of Metabolome and Bacterial Community in Whole Crop Corn Silage by Inoculating Homofermentative Lactobacillus plantarum and Heterofermentative Lactobacillus buchneri vol.9, pp.1664-302X, 2019, https://doi.org/10.3389/fmicb.2018.03299